ABSTRACT Temperature affects contractile rate properties in muscle, which may affect locomotor performance. Endotherms are known to maintain high core body temperatures, but temperatures in the periphery of the body can fluctuate. Such a phenomenon occurs in bats, whose wing musculature is relatively poorly insulated, resulting in substantially depressed temperatures in the distal wing. We examined a wing muscle in the small-bodied tropical bat Carollia perspicillata and a hindlimb muscle in the laboratory mouse at 5°C intervals from 22 to 42°C to determine the thermal dependence of the contractile properties of both muscles. We found that the bat extensor carpi radialis longus had low thermal dependence from near body temperature to 10°C lower, with Q 10 values of less than 1.5 for relaxation from contraction and shortening velocities in that interval, and with no significant difference in some rate properties in the interval between 32 and 37°C. In contrast, for all temperature intervals below 37°C, Q 10 values for the mouse extensor digitorum longus were 1.5 or higher, and rate properties differed significantly across successive temperature intervals from 37 to 22°C. An ANCOVA analysis found that the thermal dependencies of all measured isometric and isotonic rate processes were significantly different between the bat and mouse muscles. The relatively low thermal dependence of the bat muscle likely represents a downward shift of its optimal temperature and may be functionally significant in light of the variable operating temperatures of bat wing muscles.

SUMMARY We examined the hypothesis that structural features of the iliotibialis lateralis pars postacetabularis (ILPO) in guinea fowl allow this large muscle to maintain equivalent function along its anterior–posterior axis. The ILPO, the largest muscle in the hindlimb of the guinea fowl, is a hip and knee extensor. The fascicles of the ILPO originate across a broad region of the ilium and ischium posterior to the hip. Its long posterior fascicles span the length of the thigh and insert directly on the patellar tendon complex. However, its anterior fascicles are shorter and insert on a narrow aponeurosis that forms a tendinous band along the anterior edge of the muscle and is connected distally to the patellar tendon. The biarticular ILPO is actively lengthened and then actively shortened during stance. The moment arm of the fascicles at the hip increases along the anterior to posterior axis, whereas the moment arm at the knee is constant for all fascicles. Using electromyography and sonomicrometry, we examined the activity and strain of posterior and anterior fascicles of the ILPO. The activation was not significantly different in the anterior and posterior fascicles. Although we found significant differences in active lengthening and shortening strain between the anterior and posterior fascicles, the differences were small. The majority of shortening strain is caused by hip extension and the inverse relationship between hip moment arm and fascicle length along the anterior–posterior axis was found to have a major role in ensuring similar shortening strain. However, because the knee moment arm is the same for all fascicles, knee flexion in early stance was predicted to produce much larger lengthening strains in the short anterior fascicles than our measured values at this location. We propose that active lengthening of the anterior fascicles was lower than predicted because the aponeurotic tendon of insertion of the anterior fascicles was stretched and only a portion of the lengthening had to be accommodated by the active muscle fascicles.

SUMMARY The iliotibialis lateralis pars postacetabularis (ILPO) is the largest muscle in the hindlimb of the guinea fowl and is thought to play an important role during the stance phase of running, both absorbing and producing work. Using sonomicrometry and electromyography, we examined whether the ILPO experiences differential strain between proximal, central and distal portions of the posterior fascicles. When the ILPO is being lengthened while active, the distal portion was found to lengthen significantly more than either the proximal or central portions of the muscle. Our data support the hypothesis that the distal segment lengthened farther and faster because it began activity at shorter sarcomere lengths on the ascending limb of the length–tension curve. Probably because of the self-stabilizing effects of operating on the ascending limb of the length–tension curve, all segments reached the end of lengthening and started shortening at the same sarcomere length. During shortening, this similarity in sarcomere length among the segments was maintained, as predicted from force–velocity effects, and shortening strain was similar in all segments. The differential active strain during active lengthening is thus ultimately determined by differences in strain during the passive portion of the cycle. The sarcomere lengths of all segments of the fascicles were similar at the end of active shortening, but after the passive portion of the cycle the distal segment was shorter. Differential strain in the segments during the passive portion of the cycle may be caused by differential joint excursions at the knee and hip acting on the ends of the muscle and being transmitted differentially by the passive visco-elastic properties of the muscle. Alternatively, the differential passive strain could be due to the action of active or passive muscles in the thigh that transmit force to the IPLO in shear. Based on basic sarcomere dynamics we predict that differential strain is more likely to occur in muscles undergoing active lengthening at the beginning of contraction than those undergoing only shortening.

SUMMARY Physiological and anatomical evidence suggests that in birds the iliotibialis lateralis pars postacetabularis (ILPO) is functionally important for running. Incorporating regional information, we estimated the mean sarcomere strain trajectory and electromyographic (EMG) amplitude of the ILPO during level and incline walking and running. Using these data and data in the literature of muscle energy use, we examined three hypotheses: (1) active lengthening will occur on the ascending limb of the length–tension curve to avoid potential damage caused by stretch on the descending limb; (2) the active strain cycle will shift to favor active shortening when the birds run uphill and shortening will occur on the plateau and shallow ascending limb of the length–tension curve; and (3) measures of EMG intensity will correlate with energy use when the mechanical function of the muscle is similar. Supporting the first hypothesis, we found that the mean sarcomere lengths at the end of active lengthening during level locomotion were smaller than the predicted length at the start of the plateau of the length–tension curve. Supporting the second hypothesis, the magnitude of active lengthening decreased with increasing slope, whereas active shortening increased. In evaluating the relationship between EMG amplitude and energy use (hypothesis 3), we found that although increases in EMG intensity with speed, slope and loading were positively correlated with muscle energy use, the quantitative relationships between these variables differed greatly under different conditions. The relative changes in EMG intensity and energy use by the muscle probably varied because of changes in the mechanical function of the muscle that altered the ratio of muscle energy use to active muscle volume. Considering the overall function of the cycle of active lengthening and shortening of the fascicles of the ILPO, we conclude that the function of active lengthening is unlikely to be energy conservation and may instead be related to promoting stability at the knee. The work required to lengthen the ILPO during stance is provided by co-contracting knee flexors. We suggest that this potentially energetically expensive co-contraction serves to stabilize the knee in early stance by increasing the mechanical impedance of the joint.

SUMMARY Although mechanical linkages between the proximal and distal limb are present in a range of species, their functional significance is unknown. We have investigated the mechanical function of the flexor cruris lateralis pars pelvica (FCLP), flexor cruris lateralis pars accessoria (FCLA) and gastrocnemius intermedia (GI), a system of linked muscles spanning proximal and distal limb segments in the guinea fowl ( Numida meleagris ) hind limb. The FCLP, which is in the anatomical position of a hamstring muscle, is the primary component of the linkage. It is connected to the distal femur via the FCLA, the tarsometatarsus via the tendon of insertion of the GI and the common Achilles tendon, and the tibiotarsus via a distal tendon of insertion. The FCLP may, therefore, potentially exert moments at the hip, knee and ankle joints depending on the joint angles and the relative states of activation in the three muscles. Evidence presented here suggests that the GI and FCLA act as actively controlled links that alter distal action of the FCLP. The FCLP and GI are coactive in the late swing and early stance phases of the stride, forming a triarticular complex, and likely act together to resist and control ankle flexion immediately after foot-down in addition to providing hip extension and knee flexion moments. The FCLP and FCLA are coactive from mid-through to late stance, acting together as a uniarticular hip extensor. Available evidence suggests that this role of the FCLP and FCLA is of increased importance in inclined running and accelerations. This linkage between a proximal muscle and alternate distal connections allows for functional flexibility, both in terms of the site at which the muscle exerts force and the nature of the muscle's mechanical function. The interactions generated between the proximal and distal limb by linkages of this type suggest that less emphasis should be placed on the distinct functional roles of specific anatomical classes of muscle within proximal and distal limb segments.

SUMMARY Uphill running requires more energy than level running at the same speed,largely due to the additional mechanical work of elevating the body weight. We explored the distribution of energy use among the leg muscles of guinea fowl running on the level and uphill using both organismal energy expenditure(oxygen consumption) and muscle blood flow measurements. We tested each bird under four conditions: (1) rest, (2) a moderate-speed level run at 1.5 m s –1 , (3) an incline run at 1.5 m s –1 with a 15% gradient and (4) a fast level run at a speed eliciting the same metabolic rate as did running at a 15% gradient at 1.5 m s –1 (2.28–2.39 m s –1 ). The organismal energy expenditure increased by 30% between the moderate-speed level run and both the fast level run and the incline run, and was matched by a proportional increase in total blood flow to the leg muscles. We found that blood flow increased significantly to nearly all the leg muscles between the moderate-speed level run and the incline run. However, the increase in flow was distributed unevenly across the leg muscles, with just three muscles being responsible for over 50% of the total increase in blood flow during uphill running. Three muscles showed significant increases in blood flow with increased incline but not with an increase in speed. Increasing the volume of active muscle may explain why in a previous study a higher maximal rate of oxygen consumption was measured during uphill running. The majority of the increase in energy expenditure between level and incline running was used in stance-phase muscles. Proximal stance-phase extensor muscles with parallel fibers and short tendons, which have been considered particularly well suited for doing positive work on the center of mass, increased their mass-specific energy use during uphill running significantly more than pinnate stance-phase muscles. This finding provides some evidence for a division of labor among muscles used for mechanical work production based on their muscle–tendon architecture. Nevertheless, 33% of the total increase in energy use (40% of the increase in stance-phase energy use) during uphill running was provided by pinnate stance-phase muscles. Swing-phase muscles also increase their energy expenditure during uphill running, although to a lesser extent than that required by running faster on the level. These results suggest that neither muscle–tendon nor musculoskeletal architecture appear to greatly restrict the ability of muscles to do work during locomotor tasks such as uphill running, and that the added energy cost of running uphill is not solely due to lifting the body center of mass.

SUMMARY Linking the mechanics and energetics of locomotion in vertebrates has been hampered by a lack of information regarding the energy use of individual skeletal muscles in vivo . Here, we present a review of the available data concerning the relationship between the rates of skeletal muscle blood flow and oxygen consumption( V̇ O 2 ). In active muscle, during aerobically supported exercise, there is a linear relationship between these variables, irrespective of the muscle fiber type and intensity of exercise through most of the aerobic exercise range. We conclude that the rate of blood flow is the best available indicator of aerobic metabolic rate in multiple individual muscles or regions of muscles during locomotion. The practical considerations of using the injectable microsphere technique to measure muscle blood flow in this context are discussed.

SUMMARY We examined the changes in muscle energy use in guinea fowl running at 1.5 m s -1 either unloaded, or carrying trunk loads equal to 23% of body mass, or loads on their distal legs equal to a total of 5% of body mass. We estimated muscle energy use by measuring blood flow to all of the leg muscles using injected microspheres. Total blood flow to the leg muscles increased by approximately 15% under both loading conditions, which matched the percentage increase in net organismal metabolic rate. Significant increases in energy use(inferred from blood flow) above that found in unloaded birds were found in 12 muscles in trunk-loaded birds, with most of the increases restricted to stance-phase muscles, as predicted. Just three of these muscles, the femerotibialis, the iliotibialis lateralis pars postacetabularis and the fibularis longus accounted for 70% of the increased energy use. Noticeably absent from the group of muscles that increased energy use during trunk loading were several large biarticular muscles that have extensor actions at the hip or ankle, but flexor actions at the knee. We concluded that the low energetic cost of carrying trunk loads in guinea fowl may rely on the activation of a group of muscles that together provide support and propulsion across all the major joints, without producing opposing moments at other joints that could potentially waste energy. The specific leg muscles responsible for the increase in metabolism during trunk loading also suggest that the energy cost of producing mechanical work may be an important determinant of the cost of carrying extra mass on the trunk. During distal-limb loading, eleven leg muscles had significant increases in energy use, but unlike during trunk loading, both stance- and swing-phase muscles had large increases in energy use. This distribution of energy use between stance and swing agrees with the prediction that increased mechanical work determines the cost of limb loading, because a substantial fraction of the increased segmental work during distal-limb loading in guinea fowl has been found to occur during stance.

SUMMARY We examined the energetic cost of loading the trunk or distal portion of the leg in walking and running guinea fowl ( Numida meleagris ). These different loading regimes were designed to separately influence the energy use by muscles used during the stance and swing phases of the stride. Metabolic rate, estimated from oxygen consumption, was measured while birds locomoted on a motorized treadmill at speeds from 0.5 to 2.0 m s -1 , either unloaded, or with a mass equivalent to 23% of their body mass carried on their backs, or with masses equal to approximately 2.5% of their body mass attached to each tarsometatarsal segment. In separate experiments, we also measured the duration of stance and swing in unloaded, trunk-loaded, or limb-loaded birds. In the unloaded and limb-loaded birds, we also calculated the mechanical energy of the tarsometatarsal segment throughout the stride. Trunk and limb loads caused similar increases in metabolic rate. During trunk loading, the net metabolic rate (gross metabolic rate - resting metabolic rate) increased by 17% above the unloaded value across all speeds. This percentage increase is less than has been found in most studies of humans and other mammals. The economical load carriage of guinea fowl is consistent with predictions based on the relative cost of the stance and swing phases of the stride in this species. However, the available comparative data and considerations of the factors that determine the cost of carrying extra mass lead us to the conclusion that the cost of load carrying is unlikely to be a reliable indicator of the distribution of energy use in stance and swing. Both loading regimes caused small changes in the swing and/or stance durations, but these changes were less than 10%. Loading the tarsometatarsal segment increased its segmental energy by 4.1 times and the segmental mechanical power averaged over the stride by 3.8 times. The increases in metabolism associated with limb loading appear to be linked to the increases in mechanical power. The delta efficiency (change in mechanical power divided by the change in metabolic power) of producing this power increased from 11% in walking to approximately 25% in running. Although tarsometatarsal loading was designed to increase the mechanical energy during swing phase, 40% of the increase in segmental energy occurred during late stance. Thus, the increased energy demand of distal limb loading in guinea fowl is predicted to cause increases in energy use by both stance- and swing-phase muscles.

SUMMARY The ability of birds to perform effective jumps may play an important role in predator avoidance and flight initiation. Jumping can provide the vertical acceleration necessary for a rapid takeoff, which may be particularly important for ground-dwelling birds such as phasianids. We hypothesized that by making use of elastic energy storage and release, the leg muscles could provide the large power outputs needed for achieving high velocities after takeoff. We investigated the performance of the leg muscles of the guinea fowl Numida meleagris during jumping using kinematic and force-plate analyses. Comparison of the methods indicated that in this species the wings did not supply energy to power takeoff and thus all the work and power came from the leg muscles. Guinea fowl produced a peak vertical force of 5.3 times body weight. Despite having lower muscle-mass-specific power output in comparison to more specialized jumpers, guinea fowl demonstrated surprisingly good performance by producing muscle-mass-specific work outputs of 45 J kg –1 , a value approximately two thirds of the maximal expected value for skeletal muscle. The muscle-mass-specific peak power output during jumping was nearly 800 W kg –1 , which is more than twice the peak isotonic power estimated for guinea fowl leg muscles. To account for high power outputs, we concluded that energy has to be stored early in the jumps and released later during peak power production, presumably using mechanisms similar to those found in more specialized jumpers.

SUMMARY The function of many muscles during natural movements is to accelerate a mass. We used a simple model containing the essential elements of this functional system to investigate which musculoskeletal features are important for increasing the mechanical work done in a muscle-powered acceleration. The muscle model consisted of a muscle-like actuator with frog hindlimb muscle properties, operating across a lever to accelerate a load. We tested this model in configurations with and without a series elastic element and with and without a variable mechanical advantage. When total muscle shortening was held constant at 30%, the model produced the most work when the muscle operated with a series elastic element and an effective mechanical advantage that increased throughout the contraction (31 J kg -1 muscle vs 26.6 J kg -1 muscle for the non-compliant, constant mechanical advantage configuration). We also compared the model output with the dynamics of jumping bullfrogs, measured by high-speed video analysis, and the length changes of the plantaris muscle, measured by sonomicrometry. This comparison revealed that the length, force and power trajectory of the body of jumping frogs could be accurately replicated by a model of a fully active muscle operating against an inertial load, but only if the model muscle included a series elastic element. Sonomicrometer measurements of the plantaris muscle revealed an unusual, biphasic pattern of shortening, with high muscle velocities early and late in the contraction, separated by a period of slow contraction. The model muscle produced this pattern of shortening only when an elastic element was included. These results demonstrate that an elastic element can increase the work output in a muscle-powered acceleration. Elastic elements uncouple muscle fiber shortening velocity from body movement to allow the muscle fibers to operate at slower shortening velocities and higher force outputs. A variable muscle mechanical advantage improves the effectiveness of elastic energy storage and recovery by providing an inertial catch mechanism. These results can explain the high power outputs observed in jumping frogs. More generally,our model suggests how the function of non-muscular elements of the musculoskeletal system enhances performance in muscle-powered accelerations.

SUMMARY Take-off in birds at high speeds and steep angles of elevation requires a high burst power output. The mean power output of the pectoralis muscle of blue-breasted quail ( Coturnix chinensis ) during take-off is approximately 400 W kg -1 muscle, as determined using two independent methods. This burst power output is much higher than has been measured in any other cyclically contracting muscle. The power output of muscle is determined by the interactions between the physiological properties of the muscle, the stimulation regime imposed by the central nervous system and the details of the strain cycle, which are determined by the reciprocal interaction between the muscle properties and the environmental load. The physiological adaptations that enable a high power output to be achieved are those that allow the muscle to develop high stresses whilst shortening rapidly. These characteristics include a high myofibrillar density, rapid twitch contraction kinetics and a high maximum intrinsic velocity of shortening. In addition, several features of the strain cycle increase the power output of the quail pectoralis muscle. First, the muscle operates at a mean length shorter than the plateau of the length/force relationship. Second,the muscle length trajectory is asymmetrical, with 70 % of the cycle spent shortening. The asymmetrical cycle is expected to increase the power output substantially. Third, subtle deviations in the velocity profile improve power output compared with a simple asymmetrical cycle with constant lengthening and shortening rates. The high burst power outputs found in the flight muscles of quail and similar birds are limited to very brief efforts before fatigue occurs. This strong but short flight performance is well-suited to the rapid-response anti-predation strategy of these birds that involves a short flight coupled with a subsequent sustained escape by running. These considerations serve as a reminder that the maximum power-producing capacities of muscles need to be considered in the context of the in vivo situation within which the muscles operate.

SUMMARY Blue-breasted quail ( Coturnix chinensis ) were filmed during take-off flights. By tracking the position of the centre of mass of the bird in three dimensions, we were able to calculate the power required to increase the potential and kinetic energy. In addition, high-speed video recordings of the position of the wings over the course of the wing stroke, and morphological measurements, allowed us to calculate the aerodynamic and inertial power requirements. The total power output required from the pectoralis muscle was, on average, 390 W kg –1 , which was similar to the highest measurements made on bundles of muscle fibres in vitro (433 W kg –1 ), although for one individual a power output of 530 W kg –1 was calculated. The majority of the power was required to increase the potential energy of the body. The power output of these muscles is the highest yet found for any muscle in repetitive contractions. We also calculated the power requirements during take-off flights in four other species in the family Phasianidae. Power output was found to be independent of body mass in this family. However, the precise scaling of burst power output within this group must await a better assessment of whether similar levels of performance were measured across the group. We extended our analysis to one species of hawk, several species of hummingbird and two species of bee. Remarkably, we concluded that, over a broad range of body size (0.0002–5 kg) and contractile frequency (5–186 Hz), the myofibrillar power output of flight muscles during short maximal bursts is very high (360–460 W kg –1 ) and shows very little scaling with body mass. The approximate constancy of power output means that the work output varies inversely with wingbeat frequency and reaches values of approximately 30–60 J kg –1 in the largest species.

SUMMARY Sonomicrometry and electromyographic (EMG) recordings were made for the pectoralis muscle of blue-breasted quail ( Coturnix chinensis ) during take-off and horizontal flight. In both modes of flight, the pectoralis strain trajectory was asymmetrical, with 70 % of the total cycle time spent shortening. EMG activity was found to start just before mid-upstroke and continued into the downstroke. The wingbeat frequency was 23 Hz, and the total strain was 23 % of the mean resting length. Bundles of fibres were dissected from the pectoralis and subjected in vitro to the in vivo length and activity patterns, whilst measuring force. The net power output was only 80 W kg –1 because of a large artefact in the force record during lengthening. For more realistic estimates of the pectoralis power output, we ignored the power absorbed by the muscle bundles during lengthening. The net power output during shortening averaged over the entire cycle was approximately 350 W kg –1 , and in several preparations over 400 W kg –1 . Sawtooth cycles were also examined for comparison with the simulation cycles, which were identical in all respects apart from the velocity profile. The power output during these cycles was found to be 14 % lower than during the in vivo strain trajectory. This difference was due to a higher velocity of stretch, which resulted in greater activation and higher power output throughout the later part of shortening, and the increase in shortening velocity towards the end of shortening, which facilitated deactivation. The muscle was found to operate at a mean length shorter than the plateau of the length/force relationship, which resulted in the isometric stress measured at the mean resting length being lower than is typically reported for striated muscle.